The relationship among sperm global DNA methylation, telomere length, and DNA fragmentation in varicocele: a cross-sectional study of 20 cases

References

• Agarwal A, Hamada A, Esteves SC. 2012. Insight into oxidative stress in varicocele-associated male infertility: part 1. Nat Rev Urol. 9(12):678–690.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Sharma R, Harlev A, Esteves SC. 2016. Effect of varicocele on semen characteristics according to the new 2010 World Health Organization criteria: a systematic review and meta-analysis. Asian J Androl. 18(2):163–170.
   PubMed Web of Science ®Google Scholar
• Aitken RJ, De Iuliis GN. 2010. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 16(1):3–13.
   PubMed Web of Science ®Google Scholar
• Aitken RJ, De Iuliis GN, McLachlan RI. 2009. Biological and clinical significance of DNA damage in the male germ line. Int J Androl. 32(1):46–56.
   PubMedGoogle Scholar
• Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. 2014. Oxidative stress and male reproductive health. Asian J Androl. 16(1):31–38.
   PubMed Web of Science ®Google Scholar
• Al-Ali BM, Marszalek M, Shamloul R, Pummer K, Trummer H. 2010. Clinical parameters and semen analysis in 716 Austrian patients with varicocele. Urology. 75(5):1069–1073.
   PubMed Web of Science ®Google Scholar
• Al-Ali BM, Shamloul R, Pichler M, Augustin H, Pummer K. 2013. Clinical and laboratory profiles of a large cohort of patients with different grades of varicocele. Cent Eur J Urol. 66(1):71–74.
   PubMedGoogle Scholar
• Andrabi SM. 2007. Mammalian sperm chromatin structure and assessment of DNA fragmentation. J Assist Reprod Genet. 24(12):561–569.
   PubMed Web of Science ®Google Scholar
• Armstrong JS, Rajasekaran M, Chamulitrat W, Gatti P, Hellstrom WJ, Sikka SC. 1999. Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radic Biol Med. 26(7–8):869–880.
   PubMed Web of Science ®Google Scholar
• Aston KI, Punj V, Liu L, Carrell DT. 2012. Genome-wide sperm deoxyribonucleic acid methylation is altered in some men with abnormal chromatin packaging or poor in vitro fertilization embryogenesis. Fertil Steril. 97(2):285–292.
   PubMed Web of Science ®Google Scholar
• Aston KI, Uren PJ, Jenkins TG, Horsager A, Cairns BR, Smith AD, Carrell DT. 2015. Aberrant sperm DNA methylation predicts male fertility status and embryo quality. Fertil Steril. 104(6):1388–1397.e1381–e1385.
   PubMed Web of Science ®Google Scholar
• Bahreinian M, Tavalaee M, Abbasi H, Kiani-Esfahani A, Shiravi AH, Nasr-Esfahani MH. 2015. DNA hypomethylation predisposes sperm to DNA damage in individuals with varicocele. Syst Biol Reprod Med. 61(4):179–186.
   PubMed Web of Science ®Google Scholar
• Benchaib M, Ajina M, Lornage J, Niveleau A, Durand P, Guerin JF. 2003. Quantitation by image analysis of global DNA methylation in human spermatozoa and its prognostic value in in vitro fertilization: a preliminary study. Fertil Steril. 80(4):947–953.
   PubMed Web of Science ®Google Scholar
• Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A, Guerin JF. 2005. Influence of global sperm DNA methylation on IVF results. Hum Reprod. 20(3):768–773.
   PubMed Web of Science ®Google Scholar
• Benoff S, Gilbert BR. 2001. Varicocele and male infertility: part I. Preface. Hum Reprod Update. 7(1):47–54.
   PubMed Web of Science ®Google Scholar
• Blackburn EH. 1991. Structure and function of telomeres. Nature. 350(6319):569–573.
   PubMed Web of Science ®Google Scholar
• Blasco MA. 2003. Mammalian telomeres and telomerase: why they matter for cancer and aging. Eur J Cell Biol. 82(9):441–446.
   PubMed Web of Science ®Google Scholar
• Blumer CG, Fariello RM, Restelli AE, Spaine DM, Bertolla RP, Cedenho AP. 2008. Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele. Fertil Steril. 90(5):1716–1722.
   PubMed Web of Science ®Google Scholar
• Bonetti D, Martina M, Falcettoni M, Longhese MP. 2013. Telomere-end processing: mechanisms and regulation. Chromosoma. 123(1–2):57–66
   Web of Science ®Google Scholar
• Camprubí C, Salas-Huetos A, Aiese-Cigliano R, Godo A, Pons MC, Castellano G, Grossmann M, Sanseverino W, Martin-Subero JI, Garrido N, et al. 2016. Spermatozoa from infertile patients exhibit differences of DNA methylation associated with spermatogenesis-related processes: an array-based analysis. Reprod Biomed Online. 33(6):709–719.
   PubMed Web of Science ®Google Scholar
• Cariati F, Jaroudi S, Alfarawati S, Raberi A, Alviggi C, Pivonello R, Wells D. 2016. Investigation of sperm telomere length as a potential marker of paternal genome integrity and semen quality. Reprod Biomed Online. 33(3):404–411.
   PubMed Web of Science ®Google Scholar
• Cho CL, Esteves SC, Agarwal A. 2016. Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation. Asian J Androl. 18(2):186–193.
   PubMed Web of Science ®Google Scholar
• Dada R, Kumar M, Jesudasan R, Fernandez JL, Gosalvez J, Agarwal A. 2012. Epigenetics and its role in male infertility. J Assist Reprod Genet. 29(3):213–223.
   PubMed Web of Science ®Google Scholar
• Deaton AM, Bird A. 2011. CpG islands and the regulation of transcription. Genes Dev. 25(10):1010–1022.
   PubMed Web of Science ®Google Scholar
• Diamond DA, Zurakowski D, Bauer SB, Borer JG, Peters CA, Cilento BG, Paltiel HJ, Rosoklija I, Retik AB. 2007. Relationship of varicocele grade and testicular hypotrophy to semen parameters in adolescents. J Urol. 178(4 Pt 2):1584–1588.
   PubMed Web of Science ®Google Scholar
• Doerfler W. 1991. Patterns of DNA methylation–evolutionary vestiges of foreign DNA inactivation as a host defense mechanism. Biol Chem Hoppe Seyler. 372(8):557–564.
   PubMed Web of Science ®Google Scholar
• Enciso M, Muriel L, Fernández JL, Goyanes V, Segrelles E, Marcos M, Montejo JM, Ardoy M, Pacheco A, Gosálvez J. 2006. Infertile men with varicocele show a high relative proportion of sperm cells with intense nuclear damage level, evidenced by the sperm chromatin dispersion test. J Androl. 27(1):106–111.
   PubMedGoogle Scholar
• Esteves SC, Agarwal A. 2016. Afterword to varicocele and male infertility: current concepts and future perspectives. Asian J Androl. 18(2):319–322.
   PubMed Web of Science ®Google Scholar
• Farr C, Fantes J, Goodfellow P, Cooke H. 1991. Functional reintroduction of human telomeres into mammalian cells. Proc Natl Acad Sci U S A. 88(16):7006–7010.
   PubMed Web of Science ®Google Scholar
• Feinberg AP, Cui H, Ohlsson R. 2002. DNA methylation and genomic imprinting: insights from cancer into epigenetic mechanisms. Semin Cancer Biol. 12(5):389–398.
   PubMed Web of Science ®Google Scholar
• Ferlin A, Rampazzo E, Rocca MS, Keppel S, Frigo AC, De Rossi A, Foresta C. 2013. In young men sperm telomere length is related to sperm number and parental age. Hum Reprod. 28(12):3370–3376.
   PubMed Web of Science ®Google Scholar
• Ghasemian F, Mirroshandel SA, Monji-Azad S, Azarnia M, Zahiri Z. 2015. An efficient method for automatic morphological abnormality detection from human sperm images. Comput Methods Programs Biomed. 122(3):409–420.
   PubMed Web of Science ®Google Scholar
• González-Marín C, Gosálvez J, Roy R. 2012. Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int J Mol Sci. 13(11):14026–14052.
   PubMed Web of Science ®Google Scholar
• Hamada A, Esteves SC, Agarwal A. 2013. Insight into oxidative stress in varicocele-associated male infertility: part 2. Nat Rev Urol. 10(1):26–37.
   PubMed Web of Science ®Google Scholar
• Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature. 460(7254):473–478.
   PubMed Web of Science ®Google Scholar
• Hammoud SS, Purwar J, Pflueger C, Cairns BR, Carrell DT. 2010. Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril. 94(5):1728–1733.
   PubMed Web of Science ®Google Scholar
• Hassanin AM, Ahmed HH, Kaddah AN. 2018. A global view of the pathophysiology of varicocele. Andrology. 6:654–661.
   PubMed Web of Science ®Google Scholar
• Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, Sokol RZ. 2007. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS One. 2(12):e1289.
   PubMed Web of Science ®Google Scholar
• Ishikawa T, Fujisawa M. 2005. Effect of age and grade on surgery for patients with varicocele. Urology. 65(4):768–772.
   PubMed Web of Science ®Google Scholar
• Jarow JP. 2001. Effects of varicocele on male fertility. Hum Reprod Update. 7(1):59–64.
   PubMed Web of Science ®Google Scholar
• Jenkins TG, Aston KI, James ER, Carrell DT. 2017. Sperm epigenetics in the study of male fertility, offspring health, and potential clinical applications. Syst Biol Reprod Med. 63(2):69–76.
   PubMed Web of Science ®Google Scholar
• Jenkins TG, Aston KI, Trost C, Farley J, Hotaling JM, Carrell DT. 2015. Intra-sample heterogeneity of sperm DNA methylation. Mol Hum Reprod. 21(4):313–319.
   PubMed Web of Science ®Google Scholar
• Jenkins TG, Carrell DT. 2012. The sperm epigenome and potential implications for the developing embryo. Reproduction. 143(6):727–734.
   PubMed Web of Science ®Google Scholar
• Jin B, Li Y, Robertson KD. 2011. DNA methylation: superior or subordinate in the epigenetic hierarchy? Genes Cancer. 2(6):607–617.
   PubMedGoogle Scholar
• Jones PA, Baylin SB. 2002. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 3(6):415–428.
   PubMed Web of Science ®Google Scholar
• Kadioglu TC, Aliyev E, Celtik M. 2014. Microscopic varicocelectomy significantly decreases the sperm DNA fragmentation index in patients with infertility. Biomed Res Int. 2014:1–4.
   PubMedGoogle Scholar
• Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, Sasaki H, Yaegashi N, Arima T. 2007. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 16(21):2542–2551.
   PubMed Web of Science ®Google Scholar
• Koksal IT, Usta M, Orhan I, Abbasoglu S, Kadioglu A. 2003. Potential role of reactive oxygen species on testicular pathology associated with infertility. Asian J Androl. 5(2):95–99.
   PubMed Web of Science ®Google Scholar
• Krausz C, Sandoval J, Sayols S, Chianese C, Giachini C, Heyn H, Esteller M. 2012. Novel insights into DNA methylation features in spermatozoa: stability and peculiarities. PLoS One. 7(10):e44479.
   PubMed Web of Science ®Google Scholar
• Lan J, Hua S, He X, Zhang Y. 2010. DNA methyltransferases and methyl-binding proteins of mammals. Acta Biochim Biophys Sin. 42(4):243–252.
   Google Scholar
• Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 462(7271):315–322.
   PubMed Web of Science ®Google Scholar
• Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A, Sousa M. 2008. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod. 14(2):67–74.
   PubMed Web of Science ®Google Scholar
• Miyaoka R, Esteves SC. 2012. A critical appraisal on the role of varicocele in male infertility. Adv Urol. 2012:597495.
   PubMedGoogle Scholar
• Moskovtsev SI, Willis J, White J, Mullen JB. 2010. Disruption of telomere-telomere interactions associated with DNA damage in human spermatozoa. Syst Biol Reprod Med. 56(6):407–412.
   PubMed Web of Science ®Google Scholar
• Muratori M, Tamburrino L, Marchiani S, Cambi M, Olivito B, Azzari C, Forti G, Baldi E. 2015. Investigation on the origin of sperm DNA fragmentation: role of apoptosis, immaturity and oxidative stress. Mol Med. 21:109–122.
   PubMed Web of Science ®Google Scholar
• Naughton CK, Nangia AK, Agarwal A. 2001. Pathophysiology of varicoceles in male infertility. Hum Reprod Update. 7(5):473–481.
   PubMed Web of Science ®Google Scholar
• Ng HH, Bird A. 1999. DNA methylation and chromatin modification. Curr Opin Genet Dev. 9(2):158–163.
   PubMed Web of Science ®Google Scholar
• O’Donovan A, Pantell MS, Puterman E, Dhabhar FS, Blackburn EH, Yaffe K, Cawthon RM, Opresko PL, Hsueh WC, Satterfield S, et al. 2011. Cumulative inflammatory load is associated with short leukocyte telomere length in the health, aging and body composition study. PLoS One. 6(5):e19687.
   PubMed Web of Science ®Google Scholar
• O’Sullivan RJ, Karlseder J. 2010. Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol. 11(3):171–181.
   PubMed Web of Science ®Google Scholar
• Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. 2007. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol. 307(2):368–379.
   PubMed Web of Science ®Google Scholar
• Payer B, Lee JT. 2008. X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet. 42:733–772.
   PubMed Web of Science ®Google Scholar
• Peluso G, Palmieri A, Cozza PP, Morrone G, Verze P, Longo N, Mirone V. 2013. The study of spermatic DNA fragmentation and sperm motility in infertile subjects. Arch Ital Urol Androl. 85(1):8–13.
   PubMedGoogle Scholar
• Reig-Viader R, Capilla L, Vila-Cejudo M, Garcia F, Anguita B, Garcia-Caldés M, Ruiz-Herrera A. 2014. Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. Fertil Steril. 102(3):728–738.e721.
   PubMed Web of Science ®Google Scholar
• Rice JC, Allis CD. 2001. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr Opin Cell Biol. 13(3):263–273.
   PubMed Web of Science ®Google Scholar
• Rocca MS, Speltra E, Menegazzo M, Garolla A, Foresta C, Ferlin A. 2016. Sperm telomere length as a parameter of sperm quality in normozoospermic men. Hum Reprod. 31(6):1158–1163.
   PubMed Web of Science ®Google Scholar
• Roque M, Esteves SC. 2018. Effect of varicocele repair on sperm DNA fragmentation: a review. Int Urol Nephrol. 50(4):583–603.
   PubMed Web of Science ®Google Scholar
• Sakkas D, Alvarez JG. 2010. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 93(4):1027–1036.
   PubMed Web of Science ®Google Scholar
• Saleh RA, Agarwal A, Sharma RK, Said TM, Sikka SC, Thomas AJ Jr. 2003. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril. 80(6):1431–1436.
   PubMed Web of Science ®Google Scholar
• Santana VP, Furtado CLM, Molina CAF, Nobre YTDA, Ferriani RA, Reis RM. 2015. A randomized clinical trial study of the e ffects of varicocelectomy on sperm clinical analysis and DNA fragmentation: a preliminary data. Gynecol Obstet Res Open J. 2(1):29–34.
   Google Scholar
• Santana VP, Miranda-Furtado CL, de Oliveira-Gennaro FG, Dos Reis RM. 2017. Genetics and epigenetics of varicocele pathophysiology: an overview. J Assist Reprod Genet. 34(7):839–847.
   PubMed Web of Science ®Google Scholar
• Sharma R, Agarwal A, Rohra VK, Assidi M, Abu-Elmagd M, Turki RF. 2015. Effects of increased paternal age on sperm quality, reproductive outcome and associated epigenetic risks to offspring. Reprod Biol Endocrinol. 13:35.
   PubMed Web of Science ®Google Scholar
• Sheehan MM, Ramasamy R, Lamb DJ. 2014. Molecular mechanisms involved in varicocele-associated infertility. J Assist Reprod Genet. 31(5):521–526.
   PubMed Web of Science ®Google Scholar
• Shen HM, Dai J, Chia SE, Lim A, Ong CN. 2002. Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality. Hum Reprod. 17(5):1266–1273.
   PubMed Web of Science ®Google Scholar
• Shiraishi K, Matsuyama H, Takihara H. 2012. Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology. Int J Urol. 19(6):538–550.
   PubMed Web of Science ®Google Scholar
• Shiraishi K, Takihara H, Matsuyama H. 2010. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis. World J Urol. 28(3):359–364.
   PubMed Web of Science ®Google Scholar
• Smith R, Kaune H, Parodi D, Madariaga M, Rios R, Morales I, Castro A. 2006. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 21(4):986–993.
   PubMed Web of Science ®Google Scholar
• Tavalaee M, Bahreinian M, Barekat F, Abbasi H, Nasr-Esfahani MH. 2015. Effect of varicocelectomy on sperm functional characteristics and DNA methylation. Andrologia. 47(8):904–909.
   PubMed Web of Science ®Google Scholar
• Thilagavathi J, Kumar M, Mishra SS, Venkatesh S, Kumar R, Dada R. 2013. Analysis of sperm telomere length in men with idiopathic infertility. Arch Gynecol Obstet. 287(4):803–807.
   PubMed Web of Science ®Google Scholar
• Tunc O, Tremellen K. 2009. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet. 26(9–10):537–544.
   PubMed Web of Science ®Google Scholar
• Udomsinprasert W, Kitkumthorn N, Mutirangura A, Chongsrisawat V, Poovorawan Y, Honsawek S. 2016. Global methylation, oxidative stress, and relative telomere length in biliary atresia patients. Sci Rep. 6:26969.
   PubMed Web of Science ®Google Scholar
• Urdinguio RG, Bayon GF, Dmitrijeva M, Torano EG, Bravo C, Fraga MF, Bassas L, Larriba S, Fernandez AF. 2015. Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod. 30(5):1014–1028.
   PubMed Web of Science ®Google Scholar
• Vera E, Canela A, Fraga MF, Esteller M, Blasco MA. 2008. Epigenetic regulation of telomeres in human cancer. Oncogene. 27(54):6817–6833.
   PubMed Web of Science ®Google Scholar
• von Zglinicki T. 2000. Role of oxidative stress in telomere length regulation and replicative senescence. Ann N Y Acad Sci. 908:99–110.
   PubMed Web of Science ®Google Scholar
• Wang YJ, Zhang RQ, Lin YJ, Zhang RG, Zhang WL. 2012. Relationship between varicocele and sperm DNA damage and the effect of varicocele repair: a meta-analysis. Reprod Biomed Online. 25(3):307–314.
   PubMed Web of Science ®Google Scholar
• Wong JY, De Vivo I, Lin X, Fang SC, Christiani DC. 2014a. The relationship between inflammatory biomarkers and telomere length in an occupational prospective cohort study. PLoS One. 9(1):e87348.
   PubMed Web of Science ®Google Scholar
• Wong JY, De Vivo I, Lin X, Grashow R, Cavallari J, Christiani DC. 2014b. The association between global DNA methylation and telomere length in a longitudinal study of boilermakers. Genet Epidemiol. 38(3):254–264.
   PubMed Web of Science ®Google Scholar
• Wright C, Milne S, Leeson H. 2014. Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility. Reprod Biomed Online. 28(6):684–703.
   PubMed Web of Science ®Google Scholar
• Xue J, Yang J, Yan J, Jiang X, He LY, Wu T, Guo J. 2012. Abnormalities of the testes and semen parameters in clinical varicocele. Nan Fang Yi Ke Da Xue Xue Bao. 32(4):439–442.
   PubMedGoogle Scholar
• Yehezkel S, Segev Y, Viegas-Péquignot E, Skorecki K, Selig S. 2008. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum Mol Genet. 17(18):2776–2789.
   PubMed Web of Science ®Google Scholar
• Zalenskaya IA, Bradbury EM, Zalensky AO. 2000. Chromatin structure of telomere domain in human sperm. Biochem Biophys Res Commun. 279(1):213–218.
   PubMed Web of Science ®Google Scholar
• Zargooshi J. 2007. Sperm count and sperm motility in incidental high-grade varicocele. Fertil Steril. 88(5):1470–1473.
   PubMed Web of Science ®Google Scholar
• Zhang X, Lin S, Funk WE, Hou L. 2013. Environmental and occupational exposure to chemicals and telomere length in human studies. Occup Environ Med. 70(10):743–749.
   PubMed Web of Science ®Google Scholar
• Zini A, Dohle G. 2011. Are varicoceles associated with increased deoxyribonucleic acid fragmentation? Fertil Steril. 96(6):1283–1287.
   PubMed Web of Science ®Google Scholar